Genetic differentiation and inversion clines in Indian natural populations of Drosophila melanogaster.

To study the genetic differentiation and inversion clines in Indian natural populations of Drosophila melanogaster, 14 natural populations (6 from the north and 8 from the south) were screened for chromosome inversions. The chromosomal analysis revealed the presence of 23 paracentric inversions, which include 4 common cosmopolitan, 4 rare cosmopolitan, 2 recurrent endemic, and 13 unique endemic (new inversions detected for the first time) inversions. The difference in karyotype frequencies between populations from the north and south were highly significant and the level of inversion heterozygosity was higher in populations from the south. Statistically significant negative correlations were found between each of the four common cosmopolitan inversions and latitude. These findings are in accord with results from other worldwide geographic regions and show that Indian populations of D. melanogaster have undergone considerable genetic differentiation at the level of inversion polymorphism.     

Further evidence for latitudinal inversion clines in natural populations of Drosophila melanogaster from India.

Chromosomal analysis of eight Indian natural populations (six from north India and two from south India) of Drosophila melanogaster revealed the presence of 13 paracentric inversions, including one in the X chromosome. All four types of inversions--common cosmopolitan (4), rare cosmopolitan (3), recurrent endemic (2), and unique endemic (4)--were detected. The frequency of commonly occurring inversions and the level of inversion heterozygosity were found to be higher in the two southern populations. The south Indian populations are genetically more differentiated than those from the north. Also, latitudinal clines in the frequencies of the four common cosmopolitan inversions were detected. These results provide further evidence for the existence of inversion clines in Indian populations of D. melanogaster.     

Patterns of inversion polymorphism in three species of the Drosophila melanogaster species group

In Drosophila, chromosomal polymorphism due to paracentric inversions is very common and constitutes an adaptive character. The degree of chromosomal variability varies in different species and also in different populations of the same species. Chromosomal polymorphism in Indian natural populations of three species, D. melaonogaster, D. ananassae and D. bipectinata which belong to the melanogaster species group has been studied and the quantitative data on frequency of inversions have been reported. Behaviour of chromosome inversions has also been studied in laboratory conditions. The present review summarises the work done on inversion polymorphism in Indian populations of three species which clearly demonstrates that these three species vary in their patterns of inversion polymorphism and have evolved different mechanisms for adjustment to their environments although they belong to the same species group.     

Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster

When 41 populations from Africa (south of the Sahara) and Indian Ocean islands were analysed for their chromosomal inversion polymorphism, 34 rearrangements were found, including the four common cosmopolitans (In(2L)t, In(2R)NS, In(3L)P and In(3R)P), four rare cosmopolitans (In(2L)NS, In(3R)C, In(3R)Mo and In(3R)K) and six African polymorphic ('recurrent') endemics. Mean inversion frequencies per major autosome arm were positively and, generally, highly correlated to each other. There was no altitudinal nor latitudinal cline of inversion frequency, except for one African polymorphic endemic. Significant longitudinal clines were detected for In(2L)t, In(3L)P and In(3R)K; in all cases, inversion frequencies decreased eastward. Principal components analysis and ANOVA made it possible to distinguish three groups of populations. A high level of polymorphism was found in populations from west tropical Africa. The other low altitude populations from the mainland were moderately polymorphic, whereas the lowest levels of polymorphism were those of high altitude populations and of Indian Ocean islands. Moreover, some regional and local differentiation was also found. The frequency of unique autosomal inversions was not different from those found in Asia, Australia and America, but was significantly higher than that in Europe and North Africa. A West-East differentiation was also observed for the African polymorphic endemics. The present geographic pattern suggests a long, patchy evolution with restricted gene flow, followed by the modern period with numerous recent migrations linked to human transportation.     

Chromosome Inversion Polymorphisms in DROSOPHILA MELANOGASTER. I. Latitudinal Clines and Associations between Inversions in Australasian Populations

Nineteen Australasian populations of Drosophila melanogaster have been screened for chromosome inversion polymorphisms. All 15 of the inversion types found are paracentric and autosomal, but only four of these, one on each of the major autosome arms, are common and cosmopolitan. North-south clines occur, with the frequencies of all four of the common cosmopolitan inversions increasing toward the equator. These clines in the Southern Hemisphere mirror north-south clines in the Northern Hemisphere, where the frequencies of all four of the common cosmopolitan inversions again increase towards the equator.-While few of the Australasian populations show significant disequilibrium between linked common cosmopolitan inversions, those that do invariably have excesses of coupling gametes, which is consistent with other reports. We also find nonrandom associations between the two major autosomes, with the northern populations in Australasia (those with high inversion frequencies) tending to be deficient in gametes with common cosmopolitan inversions on both major autosomes, while the southern populations in Australasia (low inversion frequencies) tend to have an excess of this class of gametes.-The clines and the nonrandom associations between the two major autosomes are best interpreted in terms of selection operating to maintain the common cosmopolitan inversion polymorphisms in natural populations of D. melanogaster.     

Maintenance of a large pericentric inversion generated by the hobo transposable element in a transgenic line of Drosophila melanogaster

The impact of the hobo transposable element in the global reorganization of the Drosophila melanogaster genome has been investigated in transgenic lines generated by the injection of hobo elements into the Hikone strain, which lacked them previously. Extensive surveys of transgenic lines followed for 250 generations have identified 13 inversions with hobo inserts at most breakpoints. One of these inversions is pericentric on chromosome 2. It has been maintained in the line where it was discovered and in several sublines at frequencies from 0.19 to 0.45, generating stable chromosomal polymorphisms, similar to cosmopolitan paracentric inversions in natural populations. Individuals homozygous for this inversion were viable and fertile, allowing the creation of a new homozygous strain.     

Paracentric inversions in man

Summary The Leuven cytogenetic center experience on paracentric inversions in man is discussed. From a total of 51,000 patients, referred for constitutional chromosome analysis during the period 1970–1985, paracentric inversions were found in 18 index patients. A puzzling finding is the high incidence (26%) of mental retardation and/or congenital malformation in the inversion carrier offspring of phenotypically normal parents with identical chromosomal rearrangements. There was also a high incidence of early fetal loss in the inversion carrier parents. This finding may be explained by an increase of chromosomally unbalanced gametes which result from crossing-over in the meiotic inversion loop. Finally, the possibility of an increased tendency to non-disjunction in paracentric inversion carrier parents is discussed. The most frequent paracentric inversion was inv(3)(p13p25); it was detected in seven unrelated index patients. According to the present experience and the literature data, the breakpoints in paracentric inversions seem to occur preferentially at 1p22, 1p36, 3p13, 3p25, 7q11, and 7q22 regions.     

Are chromosomal inversions induced by transposable elements? A paradigm from the malaria mosquito Anopheles gambiae

Chromosomal rearrangements abound in nature and can be studied in detail in organisms with polytene chromosomes. In Drosophila and in Anopheline mosquitoes most speciation processes seem to be associated with the establishment of chromosomal rearrangements, particularly of paracentric inversions. It is not known what triggers inversions in natural populations. In the laboratory inversions are commonly generated by X-rays, mutagens or after the activity of certain transposable elements (TEs). The Anopheles gambiae complex is comprised of six sibling species, each one characterized by the presence of fixed paracentric inversions on their chromosomes. Two of these, An. gambiae s.s. and An. arabiensis, are the most important vectors of human malaria and are structured into sub-populations, each carrying a characteristic set of polymorphic chromosomal inversions. We have cloned the breakpoints of the naturally occurring polymorphic inversion In(2R)d' of An. arabiensis. Analysis of the surrounding sequences demonstrated that adjacent to the distal breakpoint lies a transposable element that we called Odysseus. Characteristics of Odysseus' terminal region and its cytological distribution in different strains as well as within the same strain indicate that Odysseus is an actively transposing element. The presence of Odysseus at the junction of the naturally occurring inversion In(2R)d' suggests that the inversion may be the result of the TEs activity. Cytological evidence from Drosophila melanogaster has also implicated the hobo transposable element in the generation of certain Hawaiian endemic inversions. This picture supports the hypothesis of the important role of TEs in generating natural inversions.     

Paracentric inversions in human chromosome 7

Summary A paracentric inversion (7)(q11q22) and mosaicism 46,XX/45,X was detected in a female with minor malformations. The same inversion was observed in the mother of the patient. The analysis of high resolution banded chromosmes revealed no visible imbalance in the inverted long arm of the chromosome 7. All published cases of paracentric inversions in the human chromosome 7 are reviewed and the relationship between this inversion and the occurrence of an aneuploidy of the sex chromosomes is discussed.     

Chromosomal Homology and Molecular Organization of Muller''s Elements D and E in the Drosophila Repleta Species Group

Thirty-three DNA clones containing protein-coding genes have been used for in situ hybridization to the polytene chromosomes of two Drosophila repleta group species, D. repleta and D. buzzatii. Twenty-six clones gave positive results allowing the precise localization of 26 genes and the tentative identification of another nine. The results were fully consistent with the currently accepted chromosomal homologies and in no case was evidence for reciprocal translocations or pericentric inversions found. Most of the genes mapped to chromosomes 2 and 4 that are homologous, respectively, to chromosome arms 3R and 3L of D. melanogaster (Muller's elements E and D). The comparison of the molecular organization of these two elements between D. melanogaster and D. repleta (two species that belong to different subgenera and diverged some 62 million years ago) showed an extensive reorganization via paracentric inversions. Using a maximum likelihood procedure, we estimated that 130 paracentric inversions have become fixed in element E after the divergence of the two lineages. Therefore, the evolution rate for element E is approximately one inversion per million years. This value is comparable to previous estimates of the rate of evolution of chromosome X and yields an estimate of 4.5 inversions per million years for the whole Drosophila genome.     

Sequence-based detection and breakpoint assembly of polymorphic inversions

Inversion polymorphisms have occupied a privileged place in Drosophila genetic research since their discovery in the 1920s. Indeed, inversions seem to be nearly ubiquitous, and the majority of species that have been thoroughly surveyed have been found to be polymorphic for one or more chromosomal inversions. Despite enduring interest, however, inversions remain difficult to study because their effects are often cryptic, and few efficient assays have been developed. Even in Drosophila melanogaster, in which inversions can be reliably detected and have received considerable attention, the breakpoints of only three inversions have been characterized molecularly. Hence, inversion detection and assay design remain important unsolved problems. Here, we present a method for identification and local de novo assembly of inversion breakpoints using next-generation paired-end reads derived from D. melanogaster isofemale lines. PCR and cytological confirmations demonstrate that our method can reliably assemble inversion breakpoints, providing tools for future research on D. melanogaster inversions as well as a framework for detection and assay design of inversions and other chromosome aberrations in diverse taxa.     

Genetic differentiation in natural populations of Drosophila ananassae

Inversion polymorphism has been studied in three natural populations of Drosophila ananassae. The three cosmopolitan inversions have been detected in all the three populations analysed. Some quantitative variations in the inversion frequencies seem to exist and the level of inversion heterozygosity varies between the different populations.     

Cytogenetic studies of Chironomus circumdatus from India (Diptera: Chironomidae)

Chironomus circumdatus is one of the most common and wide-spread species in India. Cytogenetic studies pertaining to the mitotic and polytene chromosomes, nucleolar organizer regions, C-banding and naturally occurring chromosomal polymorphism have been carried out for the first time in this Indian species. Altogether seven inversions comprising six paracentric and one pericentric are detected in the Indian populations. The distribution of inversions in relation to different environmental conditions is discussed.     

Paracentric inversion 11

A new familial case of paracentric inversion of chromosome 11 inv(11)(q21q23.3) ascertained by multiple abortions in a female carrier is presented. A review of the literature shows 19 further cases of paracentric inversion 11. According to the different breakpoints, the inversions of the long arm of chromosome 11 may be classified into three types.     

Paracentric inversions: a review

This review of paracentric inversions in man includes what we know of the behaviour and reproductive consequences of paracentric inversions from other species. Observations of naturally occurring inversions in several species of plants and animals and results of experiments with mutagenically induced inversions in the mouse are discussed. From a review of 184 cases, it is concluded that most of the paracentric inversions in man are harmless and that the risk of heterozygotes having a child with an unbalanced karyotype is low. However, in some cases, it is difficult, if not impossible, to distinguish between a paracentric inversion and a paracentric insertion, the risk in the latter case being about 15%. Caution is also necessary in interpreting the results of prenatal diagnosis for heterozygotes of paracentric inversions, because of the possibility of a variety of unpredictable unbalanced chromosome products.     

Chromosome inversion polymorphism in natural populations of Drosophila punjabiensis Parshad and Paika

Drosophila punjabiensis, a member of the montium subgroup of the melanogaster species group is a very common and widespread species of Drosophila in the Indian subcontinent. Analysis of different geographic populations of this species in India has revealed altogether nine paracentric inversions. The relationship between inversions and the different environmental conditions is discussed. The pattern of inversion polymorphism in D. punjabiensis and its sibling species, D. jambulina are compared.     

Study of the karyotype of the malaria mosquito]

A study of the karyotype composition of 22 geographycally removed natural populations of the malarial mosquito Anopheles messeae Fall revealed a chromosomal polymorphism characteristic of the whole species. 13 paracentric inversions were detected, no other gene arrangements being discovered. All the inversions can be divided into two classes: 1) wide spread inversions in hetero- and homozygous forms; 2) endemic ones discovered in individual populations in the form of heterozygotes. According to the presented photomap of salivary gland chromosomes, the inversion localization are as follows: IL1 (2a--4a), IL2 (1c--4a), IL3 (2a--3b), IL4 (1c--3b), IIR1 (7c--12c), IIR2 (10b--14b), IIL1 (15b--17a), IIIR1 (24a--26c), IIIR2 (23a--24c), IIIR3 (23b--25c), IIIR4 (27c--29c), IIIR5 (27d--30c), IIIL1 (34a--39d).     

The evolutionary history of human chromosome 7

We report on a comparative molecular cytogenetic and in silico study on evolutionary changes in human chromosome 7 homologs in all major primate lineages. The ancestral mammalian homologs comprise two chromosomes (7a and 7b/16p) and are conserved in carnivores. The subchromosomal organization of the ancestral primate segment 7a shared by a lemur and higher Old World monkeys is the result of a paracentric inversion. The ancestral higher primate chromosome form was then derived by a fission of 7b/16p, followed by a centric fusion of 7a/7b as observed in the orangutan. In hominoids two further inversions with four distinct breakpoints were described in detail: the pericentric inversion in the human/African ape ancestor and the paracentric inversion in the common ancestor of human and chimpanzee. FISH analysis employing BAC probes confined the 7p22.1 breakpoint of the pericentric inversion to 6.8 Mb on the human reference sequence map and the 7q22.1 breakpoint to 97.1 Mb. For the paracentric inversion the breakpoints were found in 7q11.23 between 76.1 and 76.3 Mb and in 7q22.1 at 101.9 Mb. All four breakpoints were flanked by large segmental duplications. Hybridization patterns of breakpoint-flanking BACs and the distribution of duplicons suggest their presence before the origin of both inversions. We propose a scenario by which segmental duplications may have been the cause rather than the result of these chromosome rearrangements.     

Investigation of the origins of human autosomal inversions

A significant proportion of both pericentric and paracentric inversions have recurrent breakpoints and so could either have arisen through multiple independent events or be identical by descent (IBD) with a single common ancestor. Of two common variant inversions previously studied, the inv(2)(p11q13) was genuinely recurrent while the inv(10)(p11.2q21.2) was IBD in all cases tested. Excluding these two variants we have ascertained 257 autosomal inversion probands at the Wessex Regional Genetics Laboratory. There were 104 apparently recurrent inversions, representing 35 different breakpoint combinations and we speculated that at least some of these had arisen on more than one occasion. However, haplotype analysis identified no recurrent cases among eight inversions tested, including the variant inv(5)(p13q13). The cases not IBD were shown to have different breakpoints at the molecular cytogenetic level. No crossing over was detected within any of the inversions and the founder haplotypes extended for variable distances beyond the inversion breakpoints. Defining breakpoint intervals by FISH mapping identified no obvious predisposing elements in the DNA sequence. In summary the vast majority of human inversions arise as unique events. Even apparently recurrent inversions, with the exception of the inv(2)(p12q13), are likely to be either derived from a common ancestor or to have subtly different breakpoints. Presumably the lack of selection against most inversions allows them to accumulate and disperse amongst different populations over time. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.